(PDF) Zapping the gap: Reducing the multisensory temporal binding window by means of transcranial direct current stimulation (tD

Consciousness and Cognition 35 (2015) 143–149 Contents lists available at ScienceDirect Consciousness and Cognition journal homepage: www.elsevier.com/locate/concog Zapping the gap: Reducing the multisensory temporal binding window by means of transcranial direct current stimulation (tDCS) Sharon Zmigrod a,⇑, Leor Zmigrod b a Leiden University Institute for Psychological Research & Leiden Institute for Brain and Cognition, Leiden, The Netherlands b Department of Psychology, University of Cambridge, Cambridge, United Kingdom a r t i c l e i n f o a b s t r a c t Article history: Synchrony among the senses lies at the heart of our possession of a unified conscious per- Received 21 October 2014 ception of the world. However, due to discrepancies in physical and neural information processing from different senses, the brain accommodates a limited range of temporal asynchronies between sensory inputs, i.e. the multisensory temporal binding window Keywords: (TBW). Using non-invasive brain stimulation, we sought to modulate the audio-visual Multisensory temporal binding window TBW and to identify cortical areas implicated in the conscious perception of multisensory Brain stimulation synchrony. Participants performed a simultaneity judgment task while experiencing ano- tDCS Multisensory integration dal (Experiment 1) or cathodal (Experiment 2) transcranial direct current stimulation Posterior parietal cortex (tDCS) over parietal and frontal regions. The results demonstrate that stimulating the right posterior parietal cortex significantly reduces the audio–visual TBW by approximately 30%, thereby causally linking this region to the plasticity of the TBW. This highlights a potential interventional technique for populations with a wider TBW, such as in autism and dyslexia. Ó 2015 Elsevier Inc. All rights reserved. 1. Introduction Experiencing the world in a manner that effectively integrates and intertwines the multiple streams of information com- ing from different sensory modalities is one of the most fundamental aspects of the human perceptual experience. A critical property of the coherent conscious perception of a multisensory stimulus as a unified object or event is that the sensory inputs are perceived to be synchronous in time and space. In particular, temporal coincidence has been shown to be essential in order for the brain to distinguish between a single perceptual event and an array of independent ones (de Gelder & Bertelson, 2003; Sekuler, Sekuler, & Lau, 1997). This is especially important given the discrepancies in physical attributes, sensory transduction, and neural mechanisms involved in the processing of information from different senses (Vroomen & Keetels, 2010). As a consequence, the perceptual system is built to accommodate a limited range of temporal asynchronies between multisensory inputs, suggesting the existence of a temporal window that sustains the perception of multisensory integration (Spence & Squire, 2003; van Wassenhove, Grant, & Poeppel, 2007). Within this multisensory temporal binding window (TBW), there is a higher probability that stimuli from different modalities are integrated to form a singular multi- sensory percept, despite a lack of absolute temporal simultaneity. Indeed, Zmigrod and Hommel (2011) have demonstrated ⇑ Corresponding author at: Leiden University, Department of Cognitive Psychology, 2300 RB Leiden, The Netherlands. E-mail address:

(S. Zmigrod). http://dx.doi.org/10.1016/j.concog.2015.05.012 1053-8100/Ó 2015 Elsevier Inc. All rights reserved. 144 S. Zmigrod, L. Zmigrod / Consciousness and Cognition 35 (2015) 143–149 that when participants are exposed to auditory and visual stimuli with a stimulus onset asynchrony of up to 350 ms, audio-visual binding occurs. While the flexibility of the audio-visual temporal binding window has been documented by several studies, depicting it can be influenced by exposure to audio-visual asynchrony in both infants and adults (Fujisaki, Shimojo, Kashino, & Nishida, 2004; Lewkowicz, 2010; Navarra et al., 2005), experimental manipulation of the TBW has so far only been successfully con- ducted through a perceptual training paradigm involving extensive feedback training (Powers, Hillock, & Wallace, 2009). In this paradigm, participants underwent an intensive training in a forced choice version of the audio-visual simultaneity judg- ment task, lasting a total of five hours. This method was able to narrow the size of the multisensory temporal binding win- dow, suggesting the potential for an interventional procedure to modulate the TBW. Nevertheless, no study has experimentally manipulated the TBW through neuroscientific techniques, and a lack of clarity remains regarding the brain regions and mechanisms that underlie this adaptive shrink and stretch of the multisensory temporal window of integration. The question of how the brain achieves the perception of multisensory integration, and in particular the specific brain regions that are implicated in the associated processes, is now increasingly being tackled through non-invasive brain stim- ulation methods such as transcranial magnetic stimulation (TMS; Esterman, Verstynen, & Robertson, 2007; Muggleton, Tsakanikos, Walsh, & Ward, 2007) and transcranial direct current stimulation (tDCS; for review see Bolognini & Maravita, 2011). tDCS enables modulation of neural excitability in specified cortical regions, and causes only minor irritation. By deliv- ering low-intensity electric current to the scalp via electrodes, tDCS is thought to enhance cortical excitability through ano- dal stimulation and diminish it with cathodal stimulation (Nitsche et al., 2003; Romero Lauro et al., 2014). In comparison to TMS, tDCS involves a significantly less painful experience for the participants and has fewer adverse side-effects (Paulus, 2011, 2014). Hence, studying performance on multisensory integration tasks while delivering tDCS opens up the opportunity to investigate the causal involvement of brain regions in multimodal processing, building upon the knowledge obtained from neuroimaging and behavioral studies. The present study has two primary aims; firstly, to investigate the possibility of modulating the audio-visual temporal binding window via a non-invasive brain stimulation technique, tDCS, and secondly, to identify brain regions implicated in the perception of multisensory synchrony. The experiments use an audio-visual simultaneity judgment task, which par- ticipants perform while experiencing polarized stimulation over specific cortical areas. In particular, we investigated the pos- terior parietal cortex (PPC) and the dorsolateral prefrontal cortex (DLPFC), which have been previously associated with the detection of temporal asynchrony in auditory-visual stimulus onset (Bushara, Grafman, & Hallett, 2001; for review see Calvert, 2001). In addition, neurostimulation studies have linked the DLPFC to cognitive control processes related to feature binding (Zmigrod, Colzato, & Hommel, 2014), and have demonstrated the role of the PPC in multisensory integration (Bolognini & Maravita, 2011; Zmigrod, 2014). Thus, using a non-invasive brain stimulation technique, we sought to examine the nature of this crucial yet elusive multisensory temporal binding window. 2. Methods and materials 2.1. Participants In total, 88 Leiden University students (mean age = 20 years; age range: 18–24 years; 21 men) took part in the study, which was divided into two separate experiments. In Experiment 1, anodal tDCS was delivered (n = 40), while in Experiment 2, cathodal stimulation was given (n = 48). Subjects received course credits or a financial reward for their par- ticipation. The participants were naïve to the experimental procedure and purpose of the study. All participants were right-handed as assessed by the Edinburgh Inventory (Oldfield, 1971) with normal or corrected-to-normal vision. Exclusion criteria included: history of psychiatric disorders, drug abuse, active medication, pregnancy, or susceptibility to seizures. Participants provided their written informed consent to participate in the study, in accordance with the ethical standards of the declaration of Helsinki and approval by the Ethical Committee of Leiden University. 2.2. Experimental design and stimulation procedure The study has a between-subjects design. Participants were independently recruited for Experiment 1 and 2, where each experiment was composed of four groups with different stimulation conditions. Participants were equally divided and ran- domly assigned to one of the four groups, three of which involved tDCS stimulation in distinct cortical sites: the right PPC, left PPC, and left DLPFC. All conditions involved a simultaneity judgment task. In addition, a control group performed the same task without receiving stimulation or being connected to the tDCS apparatus. In Experiment 1, tDCS was employed with anodal polarity over the designated cortical area, and in Experiment 2, cathodal stimulation was used. tDCS was delivered by means of a DC Brain Stimulator Plus (NeuroConn, Ilmenau, Germany) and was applied through a saline-soaked pair of surface sponge electrodes (5 cm 7 cm). The active electrode was placed over either P4, P3, or F3 (depending on the participant’s stimulation group), a location atop the right PPC, left PPC, and the left DLPFC respectively, according to the international 10–20 system for EEG electrode placement. The reference electrode was placed over the con- tralateral supraorbital area as this montage has been proven to be effective in neurostimulation studies involving multisen- sory perception (Bolognini, Fregni, Casati, Olgiati, & Vallar, 2010; Bolognini & Maravita, 2011; Zmigrod, 2014; Zmigrod et al., S. Zmigrod, L. Zmigrod / Consciousness and Cognition 35 (2015) 143–149 145 2014) and other cognitive functions (Cerruti & Schlaug, 2009; Javadi & Walsh, 2012; Metuki, Sela, & Lavidor, 2012; for review see Nitsche et al., 2008). The stimulation lasted 15 min with a constant current of 2 mA and with a 15-s fade-in and fade-out. For the groups undergoing tDCS, the session began with the appropriate stimulation and a practice block of 15 trials of the simultaneity judgment task. After the task was well understood and the tDCS was on for 5 min, the experimental block with 120 trials began. The order of the trials was randomized. The sequence of events in each trial is shown in Fig. 1. The control group performed the same behavioral task however experienced no stimulation and was unconnected to the tDCS apparatus. 2.3. Simultaneity judgment task The audio-visual simultaneity judgment task was based on a design by Zmigrod and Hommel (2011). The bimodal stimuli were composed of pure tones with 1000 Hz or 3000 Hz (duration 50 ms) presented at approximately 70 dB SPL, and accom- panied by a colored circle which was either red or blue. The sound preceded the color at the stimulus onset asynchronies (SOAs) of 150, 250, or 350 ms. The SOAs were used as the independent variable in relation to subjects’ judgment of simul- taneity between the sound and color. The order of the trials was randomized. The participants were instructed to judge whether the sound and color appeared ‘‘at the same time (together)’’ and then press ‘‘Z’’ (corresponding to the Dutch word ‘‘same’’; ‘‘Zelfde’’) or ‘‘not at the same time (separately)’’ and press on the ‘‘N’’ key (for the Dutch word ‘‘not the same’’; ‘‘Niet het zelfde’’). The use of two tones and two colors creates four possible combinations presented randomly to the participant, thus preventing habituation to the stimuli. Both the visual and the auditory stimuli were presented from the same spatial location, a computer screen with integrated speakers, thereby avoiding any spatial confounds. 3. Results In both Experiment 1 (anodal tDCS) and Experiment 2 (cathodal tDCS), simultaneity judgment was calculated as the per- centage of responses whereby subjects indicated the stimuli occurred at ‘‘the same time’’ for each of the SOAs (150, 250, 350 ms) (see Table 1). The effect of tDCS was assessed with one-way ANOVA to determine whether there are any significant differences between the percentages of the simultaneity judgment for the different stimulation conditions (right PPC, left PPC, left DLPFC, no stimulation) for each of the SOAs. The dependent variables were the different SOAs and the factor was the stimulation condition. A significance level of p < .05 was used. Post-hoc least significant difference (LSD) analysis was used to study the difference between the stimulation conditions. Experiment Time 5 min 10 min Start Instructions tDCS Experimental Block (120 trials) Practice Block (15 trials) Trial Auditory SOAs Visual (1000 ms) (2000 ms) (1000 ms) stimulus (150, 250, stimulus (50 ms) 350 ms) (2000 ms) Press + Z = together N = not Time Z or N Fig. 1. Experiment design: Sequence of events in an experimental session and in each trial of the Simultaneity Judgment Task. Each session begins with tDCS on the relevant cortical region, depending on the stimulation condition assigned to the participant, followed by a 5 min practice block and the 10 min experimental block. The control condition with no stimulation follows the same sequence, except for the tDCS. Each trial consists of the presentation of the auditory stimulus, with a temporal interval depending on the stimuli onset asynchrony (SOA) of that trial, followed by the presentation of the visual stimulus. The participants must then indicate whether the auditory and visual stimuli occurred simultaneously or not. 146 S. Zmigrod, L. Zmigrod / Consciousness and Cognition 35 (2015) 143–149 Table 1 Means and standard deviation of simultaneity judgment as a function of stimulated brain region for each of the stimuli onset asynchronies (SOAs) for Experiment 1 and 2. Simultaneity judgment 150 ms 250 ms 350 ms M% SD M% SD M% SD Experiment 1 anodal stimulation Right PPC 53.96 21.18 22.22 24.49 9.41 9.37 Left PPC 74.66 14.9 38.08 21.43 17.81 17.3 Left DLPFC 73.86 15.96 35.54 19.09 11.6 13.16 No stimulation 77.1 10.63 36.58 16.76 14.36 16.69 Experiment 2 cathodal stimulation Right PPC 72.16 19.24 31.71 24.37 11.59 14.69 Left PPC 74.67 12.74 23.9 21.69 12.76 19.70 Left DLPFC 68.74 15.17 27.16 17.37 7.69 8.18 No stimulation 77.0 17.18 34.05 22.72 10.42 18.56 All participants completed the task without major complaints or discomfort as measured by the tDCS Adverse Effects Questionnaire (Brunoni et al., 2011). As shown in Figs. 2 and 3, the likelihood of judging the visual and the auditory features as occurring simultaneously decreases as the temporal asynchrony increases, confirming that the behavioral task (i.e. Simultaneity Judgment Task) worked as expected. 3.1. Experiment 1: Anodal stimulation A significant main effect of the stimulation condition was observed in the synchrony judgment of the 150 ms SOA, F(3, 36) = 4.419, p < .01, (see Fig. 2). Post hoc LSD showed a significant difference between the right PPC stimulation com- pared to the control group without stimulation (p = .003), left PPC stimulation (p = .007), and left DLPFC stimulation (p = .009). Moreover, we calculated that the percentage reduction in simultaneity judgment between stimulation over the right PPC and the other stimulation conditions was 30% in relation to no stimulation, 28% in relation to left PPC, and 27% in relation to left DLPFC stimulation. This suggests that anodal stimulation over the right PPC leads to an approximately 30% decrease in simultaneity judgment between auditory and visual features in comparison to the other conditions. As depicted in Fig. 2, the simultaneity judgment for the SOAs of 250 ms and 350 ms were also reduced during right PPC stim- ulation compared to the other conditions, however these effects did not reach a significant level. 3.2. Experiment 2: Cathodal stimulation No significant differences were found between the stimulation conditions during cathodal stimulation, F < 1 for all SOAs. In comparison to Experiment 1, the simultaneity judgment scores were similar to all stimulation conditions excluding anodal right PPC stimulation, indicating the specific causal relationship between anodal stimulation over the right PPC and the audio-visual temporal binding window. 4. Discussion Our findings demonstrate that anodal tDCS over the right PPC can substantially narrow the temporal binding window (TBW) during which multisensory synchrony is perceived, thereby implicating this region in the underlying neural Experiment 1 - Anodal tDCS 90 * Simultaneity judgment % 80 70 60 50 No Stimulation 40 L-DLPFC 30 L-PPC R-PPC 20 10 0 150 ms 250 ms 350 ms SOAs between auditory and visual features Fig. 2. Experiment 1, anodal tDCS: Synchrony judgment as a function of stimulated brain region (control – no stimulation, left DLPFC, left PPC, right PPC) with anodal stimulation in Experiment 1 for each of the stimuli onset asynchronies (SOAs) examined. ⁄ p < .01. S. Zmigrod, L. Zmigrod / Consciousness and Cognition 35 (2015) 143–149 147 Experiment 2 - Cathodal tDCS 90 Simultaneity judgment % 80 70 60 50 No Stimulation 40 L-DLPFC 30 L-PPC R-PPC 20 10 0 150 ms 250 ms 350 ms SOAs between auditory and visual features Fig. 3. Experiment 2, cathodal tDCS: Synchrony judgment as a function of the stimulated region (control – no stimulation, left DLPFC, left PPC, right PPC) with cathodal stimulation in Experiment 2 for each of the stimuli onset asynchronies (SOAs) examined. mechanisms responsible for the plasticity of the audio-visual TBW. In particular, anodal stimulation over the right PPC sig- nificantly reduced the rate of audio-visual synchrony judgment by approximately 30% for an SOA of 150 ms compared to conditions without stimulation, with anodal stimulation over other cortical regions, or with cathodal stimulation. These results are in line with Powers et al., 2009 finding of a similar reduction in the width of the temporal binding window fol- lowing perceptual training. Nevertheless, rather than active feedback training spanning multiple days and sessions, we observed a comparable effect after several minutes of non-invasive brain stimulation. Moreover, utilizing tDCS to shrink the TBW requires no conscious or active involvement from the participant, suggesting it may act as an effective interven- tional technique in clinical settings. The findings emerging from the present study are the first to delineate a causal relationship between the right PPC and the width of the audio-visual temporal binding window. Previous correlational studies using neuroimaging techniques have identified neural networks involving the posterior and inferior parietal cortices that are associated with the detection of tem- poral asynchrony in audio-visual stimuli (Bushara et al., 2001; Calvert, 2001). Furthermore, for other multisensory integra- tion processes, neurostimulation studies have provided evidence for the involvement of the parietal cortex, specifically the right PPC. Recent research has demonstrated that disruption of the right PPC with TMS influences binding of auditory and visual stimuli in healthy participants (Kamke, Vieth, Cottrell, & Mattingley, 2012), and weakens synesthetic bindings of color and shape in color-grapheme synesthesia (Esterman, Verstynen, Ivry, & Robertson, 2006; Muggleton et al., 2007). The role of the PPC in multisensory integration of other modalities was also manifest in a study by Pasalar, Ro, and Beauchamp (2010), where TMS over the PPC interrupted visual-tactile integration. In addition, Zmigrod (2014) has found that tDCS delivered to the right PPC disrupts audio-visual integration, and Bolognini et al., 2010 have illustrated that anodal tDCS delivered to the right, but not left, PPC helps to facilitate performance on an audio-visual exploration training task. Thus, the current findings offer additional evidence for the causal relationship between the right PPC and the temporal binding window. Interestingly, the findings indicate that anodal, but not cathodal, stimulation over the right PPC had an effect on the tem- poral binding window. Given that anodal stimulation is thought to increase cortical excitability in the targeted brain region (Nitsche et al., 2003; Priori, 2003), it could be that stimulation of the right PPC reduced the activation threshold necessary for detecting audio-visual asynchrony at the narrow SOA interval of 150 ms. This may have subsequently led to the shrinking of the TBW needed for integration of the auditory and visual features. In contrast, although cathodal stimulation is assumed to decrease cortical excitability, no modulation effect was observed in the present study. It may be that reducing excitability does not produce a change in the temporal binding window mechanism, or alternatively it could be speculated that a stron- ger current than 2 mA may increase the TBW. Since most tDCS studies investigating multisensory integration only report the effects of anodal versus sham stimulations (Bolognini et al., 2010; for review see Bolognini & Maravita, 2011), it is challeng- ing to compare the present cathodal results to other studies. Future research in the field should seek to include data about cathodal stimulation, and to further examine the dynamic between anodal and cathodal stimulation effects in multisensory integration. Stevenson, Zemtsov, and Wallace (2012) illustrated a correlation between the width of the temporal binding window and the temporal precision of the individual’s multisensory integration such that individuals with a narrower temporal window of integration have an enhanced ability to dissociate asynchronous audio-visual inputs, and therefore are less likely to bind stimulus inputs that are asynchronous into a single percept. Hence, the TBW and the strength of an individual’s multisensory integration may be critically linked. As pointed out by Stevenson et al. (2012), this is further supported by the evidence depicting that autistic individuals possess an extended temporal window of integration (Foss-Feig et al., 2010; Kwakye, Foss-Feig, Cascio, Stone, & Wallace, 2010) in conjunction with the literature about abnormalities in the multisensory inte- gration processes of individuals with autistic spectrum disorder (ASD) (Mongillo et al., 2008; Russo et al., 2010). A similar pattern of a wide TBW and deficits in multisensory integration are observed in individuals with dyslexia (e.g. Bastien-Toniazzo, Stroumza, & Cavé, 2010) and schizophrenia (e.g. de Gelder et al., 2003; Hamm, Gilmore, Picchetti, 148 S. Zmigrod, L. Zmigrod / Consciousness and Cognition 35 (2015) 143–149 Sponheim, & Clementz, 2011). In light of our findings that localized brain stimulation with tDCS over the right PPC leads to a narrowing of the temporal window of integration, one could postulate that reducing the TBW could lead to an improvement in the accuracy of stimuli detection and to a reduction of perceptual ambiguity. Indeed, clinical neurostimulation studies have demonstrated that non-invasive brain stimulation can be used as a tool to improve symptoms of various neuropsychi- atric disorders (for review see Demirtas-Tatlidede, Vahabzadeh-Hagh, & Pascual-Leone, 2013). This technique may thereby have the potential to alleviate some of the associated deficits in multisensory temporal processing and binding, which may have far-reaching consequences for clinical interventions in neurological disorders such as ASD and dyslexia. Moreover, recent studies have indicated that as the brain develops and matures throughout the lifespan, the period of time during which intersensory temporal synchrony takes place also changes. Lewkowicz (1996) has found the auditory-visual TBW to be significantly wider in infants than adults, and therefore narrows as the individual ages. Additionally, adjustments in audio-visual temporal perception continue after the first decade of life (Hillock, Powers, & Wallace, 2011). However, in elderly individuals, the temporal window of integration is thought to expand (Diederich, Colonius, & Schomburg, 2008), which could account for or be a by-product of age-related decline in perception and cognition. Thus, the present findings could suggest interventional techniques for enhancement of perceptual abilities related to the effective fusion of sensory information and maintenance of temporal coherence, therefore calling for further research about relevant applications in clinical populations. There is still controversy regarding the use of brain stimulation as a technique for studying brain functions and mecha- nisms. On one hand, some have argued that it is imprecise due to the sizable electrodes placed on the scalp and the effect of the reference electrode’s position (Mehta, Pogosyan, Brown, & Brittain, 2014). Yet on the other hand, many have emphasized the contribution of electrical stimulation to the aim of uncovering links between specific brain regions and cognitive func- tions, as well as to the possibility of finding useful interventions for patients (for review see Nitsche & Paulus, 2000; Tehovnik, 1996; Tehovnik, Tolias, Sultan, Slocum, & Logothetis, 2006). While findings must be cautiously interpreted and dif- ferent montages should be applied in a replicable fashion, neurostimulation techniques have had significant success in clin- ical applications (Demirtas-Tatlidede et al., 2013; Nitsche & Paulus, 2000) and in generating insight into how the brain works (Ukueberuwa & Wassermann, 2010). In conclusion, as synchrony among the senses lies at the heart of our possession of a unified and efficient perception of the world, our study builds upon the theme of the unity of consciousness that runs through the core of modern cognitive neu- roscience (Cleeremans, 2003). The study demonstrates that non-invasive brain stimulation over the right posterior parietal cortex can significantly reduce the audio-visual temporal binding window, thereby critically implicating this cortical region in affecting the plasticity of the temporal binding window as well as highlighting an interventional technique for populations with a wider temporal window of integration. Given the importance of an accurate perception of the temporal structure of sensory inputs, an ability to modulate the multisensory temporal binding window could have substantial effects on the con- scious experience of the individual, and therefore the manifestation of higher-order functions. Financial disclosures The author and the co-author of this manuscript have no relevant financial or non-financial relationships or potential con- flicts of interest to disclose. Acknowledgments We thank Michiel van Esdonk, Sanne Verhoork, and Syanah Wynn, for their assistance in data collection. 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